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10. Comparative genomic analysis of six Glossina genomes, vectors of African trypanosomes

Author

Attardo, Geoffrey M, Abd-Alla, Adly MM, Acosta-Serrano, Alvaro, Allen, James E, Bateta, Rosemary, Benoit, Joshua B, Bourtzis, Kostas, Caers, Jelle, Caljon, Guy, Christensen, Mikkel B, Farrow, David W, Friedrich, Markus, Hua-Van, Aurélie, Jennings, Emily C, Larkin, Denis M, Lawson, Daniel, Lehane, Michael J, Lenis, Vasileios P, Lowy-Gallego, Ernesto, Macharia, Rosaline W, Malacrida, Anna R, Marco, Heather G, Masiga, Daniel, Maslen, Gareth L, Matetovici, Irina, Meisel, Richard P, Meki, Irene, Michalkova, Veronika, Miller, Wolfgang J, Minx, Patrick, Mireji, Paul O, Ometto, Lino, Parker, Andrew G, Rio, Rita, Rose, Clair, Rosendale, Andrew J, Rota-Stabelli, Omar, Savini, Grazia, Schoofs, Liliane, Scolari, Francesca, Swain, Martin T, Takáč, Peter, Tomlinson, Chad, Tsiamis, George, Van Den Abbeele, Jan, Vigneron, Aurelien, Wang, Jingwen, Warren, Wesley C, Waterhouse, Robert M, Weirauch, Matthew T, Weiss, Brian L, Wilson, Richard K, Zhao, Xin, and Aksoy, Serap

Subjects
Biological Sciences, Genetics, Vector-Borne Diseases, Biotechnology, Infectious Diseases, Infection, Good Health and Well Being, Animals, DNA Transposable Elements, Drosophila melanogaster, Female, Gene Expression Regulation, Genes, Insect, Genes, X-Linked, Genome, Insect, Genomics, Geography, Insect Proteins, Insect Vectors, Male, Mutagenesis, Insertional, Phylogeny, Repetitive Sequences, Nucleic Acid, Sequence Homology, Amino Acid, Synteny, Trypanosoma, Tsetse Flies, Wolbachia, Tsetse, Trypanosomiasis, Hematophagy, Lactation, Disease, Neglected, Symbiosis, Environmental Sciences, Information and Computing Sciences, Bioinformatics
Abstract

BackgroundTsetse flies (Glossina sp.) are the vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse flies are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood-specific diet by both sexes, and obligate bacterial symbiosis. This work describes the comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans, G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes), and Fusca (G. brevipalpis) which represent different habitats, host preferences, and vectorial capacity.ResultsGenomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex-linked scaffolds show increased rates of female-specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse-specific genes are enriched in protease, odorant-binding, and helicase activities. Lactation-associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other insects. Vision-associated Rhodopsin genes show conservation of motion detection/tracking functions and variance in the Rhodopsin detecting colors in the blue wavelength ranges.ConclusionsExpanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

Published
2019

14. The Glossina Genome Cluster: Comparative Genomic Analysis of the Vectors of African Trypanosomes

Author

Attardo, Geoffrey M, Abd-Alla, Adly MM, Acosta-Serrano, Alvaro, Allen, James E, Bateta, Rosemary, Benoit, Joshua B, Bourtzis, Kostas, Caers, Jelle, Caljon, Guy, Christensen, Mikkel B, Farrow, David W, Friedrich, Markus, Hua-Van, Aurélie, Jennings, Emily C, Larkin, Denis M, Lawson, Daniel, Lehane, Michael J, Lenis, Vasileios P, Lowy-Gallego, Ernesto, Macharia, Rosaline W, Malacrida, Anna R, Marco, Heather G, Masiga, Daniel, Maslen, Gareth L, Matetovici, Irina, Meisel, Richard P, Meki, Irene, Michalkova, Veronika, Miller, Wolfgang J, Minx, Patrick, Mireji, Paul O, Ometto, Lino, Parker, Andrew G, Rio, Rita, Rose, Clair, Rosendale, Andrew J, Rota-Stabelli, Omar, Savini, Grazia, Schoofs, Liliane, Scolari, Francesca, Swain, Martin T, Takáč, Peter, Tomlinson, Chad, Tsiamis, George, Van Den Abbeele, Jan, Vigneron, Aurelien, Wang, Jingwen, Warren, Wesley C, Waterhouse, Robert M, Weirauch, Matthew T, Weiss, Brian L, Wilson, Richard K, Zhao, Xin, and Aksoy, Serap

Subjects
Biological Sciences, Genetics, Infectious Diseases, Vector-Borne Diseases, Biotechnology, Infection, Good Health and Well Being
Abstract

Background: Tsetse flies (Glossina sp.) are the sole vectors of human and animal trypanosomiasis throughout sub-Saharan Africa. Tsetse are distinguished from other Diptera by unique adaptations, including lactation and the birthing of live young (obligate viviparity), a vertebrate blood specific diet by both sexes and obligate bacterial symbiosis. This work describes comparative analysis of six Glossina genomes representing three sub-genera: Morsitans (G. morsitans morsitans (G.m. morsitans), G. pallidipes, G. austeni), Palpalis (G. palpalis, G. fuscipes) and Fusca (G. brevipalpis) which represent different habitats, host preferences and vectorial capacity. Results: Genomic analyses validate established evolutionary relationships and sub-genera. Syntenic analysis of Glossina relative to Drosophila melanogaster shows reduced structural conservation across the sex-linked X chromosome. Sex linked scaffolds show increased rates of female specific gene expression and lower evolutionary rates relative to autosome associated genes. Tsetse specific genes are enriched in protease, odorant binding and helicase activities. Lactation associated genes are conserved across all Glossina species while male seminal proteins are rapidly evolving. Olfactory and gustatory genes are reduced across the genus relative to other characterized insects. Vision associated Rhodopsin genes show conservation of motion detection/tracking functions and significant variance in the Rhodopsin detecting colors in the blue wavelength ranges. Conclusions: Expanded genomic discoveries reveal the genetics underlying Glossina biology and provide a rich body of knowledge for basic science and disease control. They also provide insight into the evolutionary biology underlying novel adaptations and are relevant to applied aspects of vector control such as trap design and discovery of novel pest and disease control strategies.

Published
2019

18. Tissue-specific localization of tick-borne pathogens in ticks collected from camels in Kenya: insights into vector competence.

Author

Khogali, Rua, Bastos, Armanda, Bargul, Joel L., Getange, Dennis, Kabii, James, Masiga, Daniel, and Villinger, Jandouwe

Subjects
RICKETTSIA, TICKS, CAMELS, ANAPLASMOSIS, SALIVARY glands, HYALOMMA, AMBLYOMMA
Abstract

Background: Tick-borne pathogen (TBP) surveillance studies often use wholetick homogenates when inferring tick-pathogen associations. However, localized TBP infections within tick tissues (saliva, hemolymph, salivary glands, and midgut) can inform pathogen transmission mechanisms and are key to disentangling pathogen detection from vector competence. Methods: We screened 278 camel blood samples and 504 tick tissue samples derived from 126 camel ticks sampled in two Kenyan counties (Laikipia and Marsabit) for Anaplasma, Ehrlichia, Coxiella, Rickettsia, Theileria, and Babesia by PCR-HRM analysis. Results: Candidatus Anaplasma camelii infections were common in camels (91%), but absent in all samples from Rhipicephalus pulchellus, Amblyomma gemma, Hyalomma dromedarii, and Hyalomma rufipes ticks. We detected Ehrlichia ruminantium in all tissues of the four tick species, but Rickettsia aeschlimannii was only found in Hy. rufipes (all tissues). Rickettsia africae was highest in Am. gemma (62.5%), mainly in the hemolymph (45%) and less frequently in the midgut (27.5%) and lowest in Rh. pulchellus (29.4%), where midgut and hemolymph detection rates were 17.6% and 11.8%, respectively. Similarly, in Hy. dromedarii, R. africae was mainly detected in the midgut (41.7%) but was absent in the hemolymph. Rickettsia africae was not detected in Hy. rufipes. No Coxiella, Theileria, or Babesia spp. were detected in this study. Conclusions: The tissue-specific localization of R. africae, found mainly in the hemolymph of Am. gemma, is congruent with the role of this tick species as its transmission vector. Thus, occurrence of TBPs in the hemolymph could serve as a predictor of vector competence of TBP transmission, especially in comparison to detection rates in the midgut, from which they must cross tissue barriers to effectively replicate and disseminate across tick tissues. Further studies should focus on exploring the distribution of TBPs within tick tissues to enhance knowledge of TBP epidemiology and to distinguish competent vectors from dead-end hosts. [ABSTRACT FROM AUTHOR]

Published
2024
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22. Genome Sequence of the Tsetse Fly (Glossina morsitans): Vector of African Trypanosomiasis

Author

Initiative, International Glossina Genome, Attardo, Geoffrey M, Abila, Patrick P, Auma, Joanna E, Baumann, Aaron A, Benoit, Joshua B, Brelsfoard, Corey L, Ribeiro, José MC, Cotton, James A, Pham, Daphne QD, Darby, Alistair C, Van Den Abbeele, Jan, Denlinger, David L, Field, Linda M, Nyanjom, Steven RG, Gaunt, Michael W, Geiser, Dawn L, Gomulski, Ludvik M, Haines, Lee R, Hansen, Immo A, Jones, Jeffery W, Kibet, Caleb K, Kinyua, Johnson K, Larkin, Denis M, Lehane, Michael J, Rio, Rita VM, Macdonald, Sandy J, Macharia, Rosaline W, Malacrida, Anna R, Marco, Heather G, Marucha, Kevin K, Masiga, Daniel K, Meuti, Megan E, Mireji, Paul O, Obiero, George FO, Koekemoer, Jacobus JO, Okoro, Chinyere K, Omedo, Irene A, Osamor, Victor C, Balyeidhusa, Apollo SP, Peyton, Justin T, Price, David P, Quail, Michael A, Ramphul, Urvashi N, Rawlings, Neil D, Riehle, Michael A, Robertson, Hugh M, Sanders, Mandy J, Scott, Maxwell J, Dashti, Zahra Jalali Sefid, Snyder, Anna K, Srivastava, Tulika P, Stanley, Eleanor J, Swain, Martin T, Hughes, Daniel ST, Tarone, Aaron M, Taylor, Todd D, Telleria, Erich L, Thomas, Gavin H, Walshe, Deirdre P, Wilson, Richard K, Winzerling, Joy J, Acosta-Serrano, Alvaro, Aksoy, Serap, Arensburger, Peter, Aslett, Martin, Bateta, Rosemary, Benkahla, Alia, Berriman, Matthew, Bourtzis, Kostas, Caers, Jelle, Caljon, Guy, Christoffels, Alan, Falchetto, Marco, Friedrich, Markus, Fu, Shuhua, Gäde, Gerd, Githinji, George, Gregory, Richard, Hall, Neil, Harkins, Gordon, Hattori, Masahira, Hertz-Fowler, Christiane, Hide, Winston, Hu, Wanqi, Imanishi, Tadashi, Inoue, Noboru, Jonas, Mario, Kawahara, Yoshihiro, Koffi, Mathurin, Kruger, Adele, Lawson, Daniel, Lehane, Stella, Lehväslaiho, Heikki, Luiz, Thiago, Makgamathe, Mmule, Malele, Imna, Manangwa, Oliver, Manga, Lucien, and Megy, Karyn

Subjects
Vector-Borne Diseases, Genetics, Prevention, Infectious Diseases, Biotechnology, 2.2 Factors relating to the physical environment, Aetiology, Infection, Good Health and Well Being, Animals, Blood, Feeding Behavior, Female, Genes, Insect, Genome, Insect, Insect Proteins, Insect Vectors, Microbiota, Molecular Sequence Annotation, Molecular Sequence Data, Reproduction, Salivary Glands, Sensation, Sequence Analysis, DNA, Symbiosis, Trypanosoma, Trypanosomiasis, African, Tsetse Flies, Wolbachia, International Glossina Genome Initiative, General Science & Technology
Abstract

Tsetse flies are the sole vectors of human African trypanosomiasis throughout sub-Saharan Africa. Both sexes of adult tsetse feed exclusively on blood and contribute to disease transmission. Notable differences between tsetse and other disease vectors include obligate microbial symbioses, viviparous reproduction, and lactation. Here, we describe the sequence and annotation of the 366-megabase Glossina morsitans morsitans genome. Analysis of the genome and the 12,308 predicted protein-encoding genes led to multiple discoveries, including chromosomal integrations of bacterial (Wolbachia) genome sequences, a family of lactation-specific proteins, reduced complement of host pathogen recognition proteins, and reduced olfaction/chemosensory associated genes. These genome data provide a foundation for research into trypanosomiasis prevention and yield important insights with broad implications for multiple aspects of tsetse biology.

Published
2014

23. Aquaporins are critical for provision of water during lactation and intrauterine progeny hydration to maintain tsetse fly reproductive success.

Author

Benoit, Joshua B, Hansen, Immo A, Attardo, Geoffrey M, Michalková, Veronika, Mireji, Paul O, Bargul, Joel L, Drake, Lisa L, Masiga, Daniel K, and Aksoy, Serap

Subjects
Animals, Tsetse Flies, Water, Aquaporins, Insect Proteins, Gene Expression Profiling, Reproduction, Lactation, Pregnancy, Female, Gene Knockdown Techniques, Biological Sciences, Medical and Health Sciences, Tropical Medicine
Abstract

Tsetse flies undergo drastic fluctuations in their water content throughout their adult life history due to events such as blood feeding, dehydration and lactation, an essential feature of the viviparous reproductive biology of tsetse. Aquaporins (AQPs) are transmembrane proteins that allow water and other solutes to permeate through cellular membranes. Here we identify tsetse aquaporin (AQP) genes, examine their expression patterns under different physiological conditions (blood feeding, lactation and stress response) and perform functional analysis of three specific genes utilizing RNA interference (RNAi) gene silencing. Ten putative aquaporins were identified in the Glossina morsitans morsitans (Gmm) genome, two more than has been previously documented in any other insect. All organs, tissues, and body parts examined had distinct AQP expression patterns. Two AQP genes, gmmdripa and gmmdripb ( = gmmaqp1a and gmmaqp1b) are highly expressed in the milk gland/fat body tissues. The whole-body transcript levels of these two genes vary over the course of pregnancy. A set of three AQPs (gmmaqp5, gmmaqp2a, and gmmaqp4b) are expressed highly in the Malpighian tubules. Knockdown of gmmdripa and gmmdripb reduced the efficiency of water loss following a blood meal, increased dehydration tolerance and reduced heat tolerance of adult females. Knockdown of gmmdripa extended pregnancy length, and gmmdripb knockdown resulted in extended pregnancy duration and reduced progeny production. We found that knockdown of AQPs increased tsetse milk osmolality and reduced the water content in developing larva. Combined knockdown of gmmdripa, gmmdripb and gmmaqp5 extended pregnancy by 4-6 d, reduced pupal production by nearly 50%, increased milk osmolality by 20-25% and led to dehydration of feeding larvae. Based on these results, we conclude that gmmDripA and gmmDripB are critical for diuresis, stress tolerance and intrauterine lactation through the regulation of water and/or other uncharged solutes.

Published
2014

24. Plasmodium -associated changes in human odor attract mosquitoes

Author

Robinson, Ailie, Busula, Annette O., Voets, Mirjam A., Beshir, Khalid B., Caulfield, John C., Powers, Stephen J., Verhulst, Niels O., Winskill, Peter, Muwanguzi, Julian, Birkett, Michael A., Smallegange, Renate C., Masiga, Daniel K., Mukabana, W. Richard, Sauerwein, Robert W., Sutherland, Colin J., Bousema, Teun, Pickett, John A., Takken, Willem, Logan, James G., and de Boer, Jetske G.

Published
2018

25. Mosquito microevolution drives Plasmodium falciparum dynamics

Author

Gildenhard, Markus, Rono, Evans K., Diarra, Assetou, Boissière, Anne, Bascunan, Priscila, Carrillo-Bustamante, Paola, Camara, Djeneba, Krüger, Hanne, Mariko, Modibo, Mariko, Ramata, Mireji, Paul, Nsango, Sandrine E., Pompon, Julien, Reis, Yara, Rono, Martin K., Seda, Pamela B., Thailayil, Janis, Traorè, Alou, Yapto, Cynthia V., Awono-Ambene, Parfait, Dabiré, Roch K., Diabaté, Abdulaye, Masiga, Daniel, Catteruccia, Flaminia, Morlais, Isabelle, Diallo, Mouctar, Sangare, Djibril, and Levashina, Elena A.

Published
2019
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33. Evidence-based advice on timing and location of tsetse control measures in Shimba Hills National reserve, Kenya

Author

Gachoki, S., Groen, T., Vrieling, A., Skidmore, A., Masiga, Daniel, GeoHealth, Department of Natural Resources, UT-I-ITC-FORAGES, Faculty of Geo-Information Science and Earth Observation, and Digital Society Institute

Subjects
ITC-ISI-JOURNAL-ARTICLE, ITC-GOLD
Abstract

Controlling tsetse flies is critical for effective management of African trypanosomiasis in Sub-Saharan Africa. To enhance timely and targeted deployment of tsetse control strategies a better understanding of their temporal dynamics is paramount. A few empirical studies have explained and predicted tsetse numbers across space and time, but the resulting models may not easily scale to other areas. We used tsetse catches from 160 traps monitored between 2017 and 2019 around Shimba Hills National Reserve in Kenya, a known tsetse and trypanosomiasis hotspot. Traps were divided into two groups: proximal ( 1.0 km) from the outer edge of the reserve boundary. We fitted zero-inflated Poisson and generalized linear regression models for each group using as temporal predictors rainfall, NDVI (Normalized Difference Vegetation Index), and LST (land surface temperature). For each predictor, we assessed their relationship with tsetse abundance using time lags from 10 days up to 60 days before the last tsetse collection date of each trap. Tsetse numbers decreased as distance from the outside of reserve increased. Proximity to croplands, grasslands, woodlands, and the reserve boundary were the key predictors for proximal traps. Tsetse numbers rose after a month of increased rainfall and the following increase in NDVI values but started to decline if the rains persisted beyond a month for distant traps. Specifically, tsetse flies were more abundant in areas with NDVI values greater than 0.7 for the distant group. The study suggests that tsetse control efforts beyond 1.0 km of the reserve boundary should be implemented after a month of increased rains in areas having NDVI values greater than 0.7. To manage tsetse flies effectively within a 1.0 km radius of the reserve boundary, continuous measures such as establishing an insecticide-treated trap or target barrier around the reserve boundary are needed.

Published
2023

45. Evaluating the efficacy of Mazao Tickoff (Metarhizium anisopliae ICIPE 7) in controlling natural tick infestations on cattle in coastal Kenya: Study protocol for a randomized controlled trial

Author

Oundo, Joseph Wang’ang’a, primary, Masiga, Daniel, additional, Okal, Michael Nyang’anga, additional, Bron, Gebbiena M., additional, Akutse, Komivi S., additional, Subramanian, Sevgan, additional, Bosch, Quirine ten, additional, Koenraadt, Constantianus J. M., additional, and Kalayou, Shewit, additional

Published
2022
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47. The COMBAT project: controlling and progressively minimizing the burden of vector-borne animal trypanosomosis in Africa

Author

Boulangé, Alain, primary, Lejon, Veerle, additional, Berthier, David, additional, Thévenon, Sophie, additional, Gimonneau, Geoffrey, additional, Desquesnes, Marc, additional, Abah, Samuel, additional, Agboho, Prudenciène, additional, Chilongo, Kalinga, additional, Gebre, Tsegaye, additional, Fall, Assane Gueye, additional, Kaba, Dramane, additional, Magez, Stefan, additional, Masiga, Daniel, additional, Matovu, Enock, additional, Moukhtar, Aldjibert, additional, Neves, Luis, additional, Olet, Pamela A., additional, Pagabeleguem, Soumaïla, additional, Shereni, William, additional, Sorli, Brice, additional, Taioe, Moeti O., additional, Tejedor Junco, María Teresa, additional, Yagi, Rehab, additional, Solano, Philippe, additional, and Cecchi, Giuliano, additional

Published
2022
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50. Comparative diagnostic and analytical performance of PCR and LAMP-based trypanosome detection methods estimated using pooled whole tsetse flies and midguts

Author

Malele, Imna I., Ouma, Johnson O., Enyaru, John C.K., Matovu, Enock, Alibu, Vincent, Auma, Joanna E., Onyoyo, Samuel G., Bateta, Rosemary, Changasi, Robert E., Mukiria, Phoebe W., Ndung’u, Kariuki, Gitonga, Purity K., Mwaniki, Lilian M., Nyingilili, Hamisi S., Lyaruu, Eugene A., Kapange, Lupakisyo A., Kamau, Peter Kuria, and Masiga, Daniel K.

Published
2013
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